The Cyclical Development of Trypanosoma vivax in the Tsetse Fly Involves an Asymmetric Division

Ooi, Cher-Pheng; Schuster, Sarah; Travaillé, Christelle; Bertiaux, Éloïse; Cosson, Alain; Goyard, Sophie; Perrot, Sylvain; Rotureau, Brice

doi:10.3389/fcimb.2016.00115

Cited by 28 publications

(26 citation statements)

References 39 publications

(82 reference statements)

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“…brucei and T . vivax , asymmetric division enables the rearrangement of cellular organelles ( Fig 1 ) necessary for the trypomastigote-epimastigote transitions that are an intrinsic part of the developmental cycle in tsetse [ 3 – 5 ]. Here we focus on the trypomastigote-epimastigote transition in the related African tsetse-transmitted trypanosome, T .…”

Section: Introductionmentioning

confidence: 99%

Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus

et al. 2018

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Trypanosomatids such as Leishmania and Trypanosoma are digenetic, single-celled, parasitic flagellates that undergo complex life cycles involving morphological and metabolic changes to fit them for survival in different environments within their mammalian and insect hosts. According to current consensus, asymmetric division enables trypanosomatids to achieve the major morphological rearrangements associated with transition between developmental stages. Contrary to this view, here we show that the African trypanosome Trypanosoma congolense, an important livestock pathogen, undergoes extensive cell remodelling, involving shortening of the cell body and flagellum, during its transition from free-swimming proventricular forms to attached epimastigotes in vitro. Shortening of the flagellum was associated with accumulation of PFR1, a major constituent of the paraflagellar rod, in the mid-region of the flagellum where it was attached to the substrate. However, the PFR1 depot was not essential for attachment, as it accumulated several hours after initial attachment of proventricular trypanosomes. Detergent and CaCl2 treatment failed to dislodge attached parasites, demonstrating the robust nature of flagellar attachment to the substrate; the PFR1 depot was also unaffected by these treatments. Division of the remodelled proventricular trypanosome was asymmetric, producing a small daughter cell. Each mother cell went on to produce at least one more daughter cell, while the daughter trypanosomes also proliferated, eventually resulting in a dense culture of epimastigotes. Here, by observing the synchronous development of the homogeneous population of trypanosomes in the tsetse proventriculus, we have been able to examine the transition from proventricular forms to attached epimastigotes in detail in T. congolense. This transition is difficult to observe in vivo as it happens inside the mouthparts of the tsetse fly. In T. brucei, this transition is achieved by asymmetric division of long trypomastigotes in the proventriculus, yielding short epimastigotes, which go on to colonise the salivary glands. Thus, despite their close evolutionary relationship and shared developmental route within the vector, T. brucei and T. congolense have evolved different ways of accomplishing the same developmental transition from proventricular form to attached epimastigote.

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Section: Introductionmentioning

confidence: 99%

Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus

et al. 2018

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“…It is also known that African trypanosomes can exhibit both types of body segregation during tsetse fly development, which could be related to colonization of salivary gland and maintenance of parasite's lifespan (symmetric division) and production of premetacyclic trypomastigotes (asymmetric division) (Ooi et al. ; Rotureau et al. ; Sharma et al.…”

Section: Discussionmentioning

confidence: 99%

“…The features of the symmetric and asymmetric divisions observed in our study were previously documented ex vivo and in vitro for two species of fish trypanosomes: Trypanosoma phaleri and T. catostomi (Jones and Woo 1991a,b). It is also known that African trypanosomes can exhibit both types of body segregation during tsetse fly development, which could be related to colonization of salivary gland and maintenance of parasite's lifespan (symmetric division) and production of premetacyclic trypomastigotes (asymmetric division) (Ooi et al 2016;Rotureau et al 2012;Sharma et al 2008). Further, T. cruzi trypomastigotes differentiate into amastigotes in mammalian host by asymmetric division (Kurup and Tarleton 2014).…”

Section: Discussionmentioning

confidence: 99%

In Vitro Cellular Division of Trypanosoma abeli Reveals Two Pathways for Organelle Replication

Borges

Toledo

Fermino³

et al. 2018

J Eukaryotic Microbiology

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Since the observation of the great pleomorphism of fish trypanosomes, in vitro culture has become an important tool to support taxonomic studies investigating the biology of cultured parasites, such as their structure, growth dynamics, and cellular cycle. Relative to their biology, ex vivo and in vitro studies have shown that these parasites, during the multiplication process, duplicate and segregate the kinetoplast before nucleus replication and division. However, the inverse sequence (the nucleus divides before the kinetoplast) has only been documented for a species of marine fish trypanosomes on a single occasion. Now, this previously rare event was observed in Trypanosoma abeli, a freshwater fish trypanosome. Specifically, from 376 cultured parasites in the multiplication process, we determined the sequence of organelle division for 111 forms; 39% exhibited nucleus duplication prior to kinetoplast replication. Thus, our results suggest that nucleus division before the kinetoplast may not represent an accidental or erroneous event occurring in the main pathway of parasite reproduction, but instead could be a species-specific process of cell biology in trypanosomes, such as previously noticed for Leishmania. This "alternative" pathway for organelle replication is a new field to be explored concerning the biology of marine and freshwater fish trypanosomes.

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“…Indeed, T. congolense transcripts upregulated at peak parasitemia frequently belong to T. congolense-specific groups, such as surface phylome family 22 members [79]. Orthologues of PAD proteins are identifiable in T. congolense, with up to 73% amino acid sequence identity, although their role in development is not defined; PAD orthologues are not identifiable in T. vivax [46] where tsetse development is restricted to the mouthparts [80].…”

Section: Preadaptation Of Bloodstream-form Parasites For Tsetse Uptakementioning

confidence: 99%

A Leap Into the Unknown – Early Events in African Trypanosome Transmission

Szöőr

Silvester

Matthews

2020

Trends in Parasitology

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HighlightsAfrican trypanosomes are mainly transmitted by tsetse flies.During uptake in a blood meal, T. brucei can use several potential environmental cues to stimulate the initiation of differentiation.Signal transduction involves a phosphatase signaling cascade and spatial control of key regulatory proteins.Once differentiation is initiated, several gene regulatory processes control the differentiation from bloodstream to tsetse midgut procyclic forms.T. brucei and T. congolense show a similar route of establishment in the tsetse gut but show different developmental mechanisms.

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The Cyclical Development of Trypanosoma vivax in the Tsetse Fly Involves an Asymmetric Division

Cited by 28 publications

References 39 publications

Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus

Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus

In Vitro Cellular Division of Trypanosoma abeli Reveals Two Pathways for Organelle Replication

A Leap Into the Unknown – Early Events in African Trypanosome Transmission

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